Last week, "The giant tortoise's tale" described ancestral tortoises floating inadvertently across from South America, colonising the Galápagos Islands by mistake, subsequently evolving local differences on each island and giant size on all of them. But why assume that the coloniser was a land tortoise? Wouldn't it be simpler to guess that marine turtles, already at home in the sea, hauled up on the island beaches as if to lay their eggs, enjoyed what they saw, stayed on dry land and evolved into tortoises? No. Nothing like that happened on the Galápagos islands, which have only been in existence a few million years.

Something very like it did happen, however, much longer ago in the ancestry of all tortoises. But that anticipates the climax to the turtle's tale - the second of my three new tales. By the way, the word turtle is a tiresome example of Bernard Shaw's observation: England and America are two countries divided by a common language. In British usage, turtles live in water and tortoises on land. For Americans, tortoises are those turtles that live on land.

There is good evidence that the most recent common ancestor of all today's tortoises, including those on the mainlands of America, Australia, Africa and Eurasia, as well as the giants of Galápagos, Aldabra, the Seychelles and other oceanic islands, was itself a land tortoise. In their recent ancestry, to misquote Stephen Hawking, it's tortoises all the way down. The various giant tortoises of the Galápagos islands are certainly descended from South American land tortoises.

If you go back far enough everything lived in the sea: watery alma mater of all life. At various points in evolutionary history, enterprising individuals within many different animal groups moved out onto the land, sometimes even to the most parched deserts, taking their own private sea water with them in blood and cellular fluids. In addition to the reptiles, birds, mammals and insects which we see all around us, other groups that have succeeded out of water include scorpions, snails, crustaceans such as woodlice and land crabs, millipedes and centipedes, spi ders and their kin and various worms. And we mustn't forget the plants, without whose prior invasion of the land none of the other migrations could have happened.

Moving from water to land involved a major redesign of every aspect of life, from breathing to reproduction: it was a great trek through biological space. Nevertheless, with what seems almost like perversity, a good number of thoroughgoing land animals later turned around, abandoned their hard-earned terrestrial re-tooling, and trooped back into the water again. Seals and sea lions (such as the breathtakingly tame Galápagos sea lion) have only gone part-way back. They show us what the intermediates might have been like, on the way to extreme cases such as whales and dugongs. Whales (including the small whales we call dolphins), and dugongs with their close cousins the manatees, ceased to be land creatures altogether and reverted to the full marine habits of their remote ancestors. They don't even come ashore to breed. They do, however, still breathe air, having never developed anything equivalent to the gills of their earlier marine incarnation.

Other animals that have returned from land to water are pond snails, water spiders, water beetles, Galápagos flightless cormorants, penguins (Galápagos has the only penguins in the northern hemisphere), marine iguanas (found nowhere but Galápagos) and turtles (abundant in the surrounding waters).

Iguanas are adept at surviving accidental oceanic crossings on driftwood (well-documented within the West Indies), and there can be no doubt that the marine iguanas of Galápagos trace back to just such a piece of living flotsam from South America. The oldest of the existing Galápagos Islands is no older than 3m years. Since the marine iguanas evolved here and nowhere else, you might think this sets a maximum limit on the date of their return to the water. The story is more complicated, however.

The Galápagos islands were made, one after the other, as the Nazca tectonic plate moved, at about 10 cm per year, over a particular volcanic hotspot under the Pacific Ocean. As the plate moved east, from time to time the hotspot punched through, delivering another island along the production line. This is why the youngest islands are towards the west and the oldest to the east. But, at the same time as the Nazca plate continues to move east, it is also being subducted under the South American plate. The easternmost islands sink under the sea, at a rate of about one centimetre per year. It is now known that, although the oldest existing island is only 3m years old, there has been an eastward-moving and sinking archipelago in this area for at least 17m years. Islands now submerged could have provided the initial haven for iguanas to colonise and evolve, at any time during that period. There would have been plenty of time for them to island-hop before their original ancestral island sank beneath the waves.

Turtles went back to the sea much longer ago. They are, in one respect, less fully given back to the water than whales or dugongs, for turtles still lay their eggs on beaches. Like all vertebrate returnees to the water, they breathe air, but in this department they go one better than whales. Some turtles extract additional oxygen from the water through a pair of chambers at the rear end, richly supplied with blood vessels. One Australian river turtle, indeed, gets the majority of its oxygen by breathing, as an Australian would not hesitate to say, through its arse.

There is evidence that all modern turtles are descended from a terrestrial ancestor who lived before most of the dinosaurs. There are two key fossils called Proganochelys quenstedti and Palaeochersis talampayensis dating from early dinosaur times, which appear to be close to the ancestry of all modern turtles and tortoises. You might wonder how we tell whether fossil animals, especially if only fragments are found, lived on land or in water. Sometimes it's pretty obvious. Ichthyosaurs were reptilian contemporaries of the dinosaurs, with fins and streamlined bodies. The fossils look like dolphins and they surely lived like dolphins, in the water. With turtles it is a little less obvious. One neat way to tell is by measuring the bones of their forelimbs.

Walter Joyce and Jacques Gauthier, at Yale University, took three key measurements in the arm and hand bones of 71 species of living turtles and tortoises. They used a kind of triangular graph paper to plot the three measurements against one another. Lo and behold, all the land tortoise species formed a tight cluster of points in the upper part of the triangle; all the water turtles cluster in the lower part of the triangular graph. There was no overlap, except when they added some species that spend time in both water and land. Sure enough, these amphibious species show up, on the triangular graph, half way between the "wet cluster" and the "dry cluster". Well then, to the obvious next step: where do the fossils fall? The hands of P. quenstedti and P. talampayensis leave us in no doubt. Their points on the graph are right in the thick of the dry cluster. Both these fossils were dry-land tortoises. They come from the era before our turtles returned to the water.

You might think, therefore, that modern land tortoises have probably stayed on land ever since those early terrestrial times, as most mammals did after a few of them went back to sea. But apparently not. If you draw out the family tree of all modern turtles and tortoises, nearly all the branches are aquatic. Today's land tortoises constitute a single branch, deeply nested among branches consisting of aquatic turtles. This suggests that modern land tortoises have not stayed on land continuously since the time of P. quenstedti and P. talampayensis . Rather, their ancestors were among those who went back to the water, and they then re-emerged back onto the land in (relatively) more recent times.

Tortoises therefore represent a remarkable double return. In common with all mammals, reptiles and birds, their remote ancestors were marine fish and before that various more or less worm-like creatures stretching back, still in the sea, to the primeval bacteria. Later ancestors lived on land and stayed there for a very large number of generations. Later ancestors still evolved back into the water and became sea turtles. And finally they returned yet again to the land as tortoises, some of which, though not the Galápagos giants, now live in the driest of deserts.

I have described DNA as "the Genetic Book of the Dead". Because of the way natural selection works, there is a sense in which the DNA of an animal is a textual description of the worlds in which its ancestors were naturally selected. For a fish, the genetic book of the dead describes ancestral seas. For us and most mammals, the early chapters of the book are all set in the sea and the later ones all out on land. For whales, dugongs, marine iguanas, penguins, seals, sea lions, turtles and, remarkably, tortoises, there is a third section of the book which recounts their epic return to the proving grounds of their remote past, the sea. But for the tortoises, perhaps uniquely, there is yet a fourth section of the book devoted to a final - or is it? - reemergence, yet again to the land. Can there be another animal for whom the genetic book of the dead is such a palimpsest of multiple evolutionary U-turns?

· Richard Dawkins's latest book, The Ancestor's Tale, is a Chaucerian pilgrimage to the evolutionary past. The pilgrims are living creatures, and their tales are used to illustrate some general principles of evolution. This essay would have been included in the book if the author had written it after, instead of before his personal pilgrimage to the islands. Next week: the lava lizard's tale.